Ingestion of microplastics by free-living marine nematodes, especially Enoplolaimus spp., in Mallipo Beach, South Korea
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Plankton Benthos Res 16(2): 109–117, 2021
Plankton & Benthos
Research
© The Japanese Association of Benthology
Ingestion of microplastics by free-living marine
nematodes, especially Enoplolaimus spp., in
Mallipo Beach, South Korea
Teawook Kang1, Dongsung Kim2,* & Je Hyeok Oh2
1
Marine Research Center, National Park Research Institute, Korea National Park Service Yeosu 59723, Republic of Korea
2
Marine Ecosystem Research Center, KIOST, 385 Haeyang-ro, Yeongdo-Gu, Busan 49111, Republic of Korea
Received 8 April 2020; Accepted 28 October 2020 Responsible Editor: Motohiro Shimanaga
doi: 10.3800/pbr.16.109
Abstract: Many plastics cause pollution in the marine environment, with microplastics (0.1 µm–5 mm) representing
a key research focus. The number of microplastics in sediments may increase rapidly, affecting organisms inhabiting
marine sediments. The aim of this study was to determine how microplastics affect nematodes in intertidal sand. We
assessed: (1) intake of microplastic particles (10 µm, 5 µm, 1 µm, or 0.5 µm) by Enoplolaimus spp. over 48 h; (2) mi-
croplastic intake by nematodes depending on feeding type (selective deposit feeders, non-selective deposit feeders, epi-
strate feeders, or predators/omnivores) over 48 h; and (3) microplastic egestion by Enoplolaimus spp. The proportion
of Enoplolaimus spp. individuals containing microplastics was significantly less in the 10-µm microplastic treatment
than in the treatments where Enoplolaimus spp. were exposed to microplastic particles of smaller sizes (5 µm, 1 µm,
or 0.5 µm). The ingestion rates of microplastics by predators/omnivores, non-selective deposit feeders, and selective
deposit feeders increased as the size of the microplastic decreased. After transferring Enoplolaimus spp. to filtered
seawater following microplastic ingestion, the proportion of Enoplolaimus spp. individuals containing the smallest size
microplastic (0.5 µm) decreased by 15% of the ingested amount in 3 days. In conclusion, there was a significant differ-
ence among microplastic-size treatments, but not among feeding types or in the interaction between microplastic size
and feeding type. The size of microplastics, rather than feeding type of nematodes, impacted ingestion rates. It is pos-
sible that microplastics in the sediment are ingested by nematodes living in marine benthic ecosystems.
Key words: egestion, ingestion, meiofauna, microplastic, nematodes
Additionally, approximately 18% of the plastic waste found
Introduction
in the ocean environment is associated with the fishing
Plastic is an important and widely used material, from industry, with aquaculture also being a significant con-
the production of basic goods (such as clothes and cosmet- tributor to plastic debris in the oceans (Hinojosa & Thiel
ics) to complicated and high-tech products (such as aircraft 2009).
and rocket nozzles). In the medical industry, plastic goods Many plastics are transported to sediments in the ma-
are crucial as aseptic and disposable materials (Hamid et rine environment (van Cauwenberghe et al. 2015b). Marine
al. 2018). Plastics are excellent packaging materials be- plastic debris represents one of the most serious environ-
cause of their low cost, excellent oxygen/moisture barrier mental issues worldwide, with microplastics being the pri-
properties, bio-inertness, and light weight (Andrady 2011). mary focus of many studies (Thompson et al. 2004, Eer-
Annual global plastic production is continuously rising and kes-Medrano et al. 2015, Rochman et al. 2016, Galloway
reaching 348 million tons in 2017 (PlasticsEurope 2018), et al. 2017). Microplastics are generally defined as being
and, as of 2010, 5–13% of this annual plastic production 0.1 µm–5 mm in diameter (Thompson et al. 2004, Moore
ended up in the marine environment (Jambeck et al. 2015). 2008) and in the marine environment, can be divided into
two components: (1) primary microplastics that are manu-
factured directly for various consumer and industrial ap-
* Corresponding author: Dongsung Kim; E-mail, dskim@kiost.ac.kr plications, and (2) secondary microplastics from the break-
110 T. Kang et al. down of larger plastic items through decomposition, such ameter
Ingestion and egestion of MPs by marine nematodes 111
in the dark. After 48 h, seawater containing Enoplolaimus
Microplastics
spp. in a petri dish was placed in a sieve with a 38 µm
We experimented with fluorescent polystyrene micro- mesh size. To remove the microplastics from the surface of
plastics to identify microplastics in the nematode body Enoplolaimus spp., they were washed using a water spray
under a fluorescence microscope. Fluorescent polysty- containing fresh water. Then, the remaining Enoplolaimus
rene microplastics (FLUOR Polystyrene; MAGSPHERE, spp. in the sieve were transferred to a petri dish and fixed
Pasadena, CA, USA), used in all experiments, are com- with formalin. Enoplolaimus spp. were mounted on micro-
mercially available and were made with fluorescent scope slides to check and identify ingested microplastics
dye (yellow-green color). Four diameters of microplas- by using fluorescence microscopy.
tics were used: 10 µm (4.57×107 particles ml−1), 5 µm Experiment 2-Microplastic intake of nematodes,
(3.65×108 particles ml−1), 1 µm (4.57×1010 particles ml−1), depending on feeding type
and 0.5 µm (3.65×1011 particles mL−1). The specific gravity In the second experiment, the feeding type of nematodes
of the microplastics used in this study was 1.05. Therefore, was evaluated in relation to the microplastic ingestion rate.
the microplastics used in the experiment sink by specific Twelve acrylic cores were collected for this analysis. All
gravity, because the density of the microplastic is greater nematodes from one acrylic core were separated and trans-
than that of seawater. ferred to a petri dish (i.e., there were 12 petri dishes each
containing the nematodes from one sediment sample).
Experimental design
The seawater and living nematodes used in Experiment
Experiment 1-Microplastic intake by Enoplolaimus spp. 2 were collected and extracted in the same way as in Ex-
In the first experiment, Enoplolaimus spp. were used periment 1. The nematodes selected for Experiment 2 were
to investigate how different sizes of microplastics affected transferred to filtered seawater to confirm movement. The
ingestion rates. Before the experiment, we analyzed sedi- nematodes were then transferred to a petri dish contain-
ment in the intertidal zone of Mallipo Beach to identify ing 5 mL of seawater. In each petri dish, approximately
the dominant nematode. Enoplolaimus was the dominant 100 nematodes sorted from one sediment sample were con-
nematode genus at the sampling site and could be distin- tained. One microliter of microplastic (10 µm, 5 µm, 1 µm,
guished under a dissecting microscope owing to its large and 0.5 µm) was added to the petri dishes (three replicates
size. In addition, the feeding type of Enoplolaimus spp. for each microplastic size). The petri dishes were stored at
is carnivorous/predator, and it has a large mouth through 20°C in the dark.
which 10 µm sized microplastics can enter. After 48 h, all nematodes were removed using a fine
Enoplolaimus spp. were separated from the collected pin under a stereoscopic microscope, transferred from for-
sediments. We put the collected sediments containing liv- malin to 3% glycerin, and then mounted on stereoscopic
ing meiofauna in 500-ml bottles. To anesthetize living microscope slides in anhydrous glycerine for identifica-
meiofauna, seawater containing 5% MgCl2 was added to tion. Nematodes were identified to the genus level by us-
the bottles containing sediments. The bottles were then ing the pictorial keys of Platt & Warwick (1983, 1988)
left for approximately 15 min to anesthetize the meiofauna. and Warwick et al. (1998), with the aid of a microscope
The bottle was stirred with a spoon so that the meiofauna (Olympus BX51, Tokyo, Japan). The nematodes that had
would float to the surface, and the supernatant containing ingested microplastics were identified using fluorescence
the meiofauna was poured into a 63 µm sieve. The nema- microscopy. The mounted nematodes were classified ac-
todes in the sieve were transferred to a petri dish. using a cording to the original groupings of Wieser (1953) into
spray with seawater containing 5% MgCl2. Next, the nem- four feeding groups: (1A) selective deposit feeders, (1B)
atodes were distinguished from other meiofauna under a non-selective deposit feeders, (2A) epistrate feeders, and
dissecting microscope by using a hook or O-type loop, and (2B) predators/omnivores.
they were confirmed to have been anesthetized (i.e., there Experiment 3-Microplastic egestion of Enoplolaimus spp.
was no movement). In Experiment 3, we investigated whether the micro-
Enoplolaimus spp. were then separated from other plastics ingested by Enoplolaimus spp. were egested. We
nematodes under a microscope by using a hook-or O-type allowed the Enoplolaimus spp. to ingest microplastics, then
loop. The selected Enoplolaimus spp. were transferred to moved them to filtered seawater for incubation for 24 and
a petri dish containing clean filtered seawater to ensure 72 h. We then measured the amount of microplastics in
that they were alive and moving. As Enoplolaimus spp. the nematodes immediately after removal from the water
emerged from anesthesia, they began to move. Twenty live containing microplastics and after 24 h and 72 h of incuba-
Enoplolaimus spp. were placed on each of 16 petri dish- tion in the filtered seawater. A total of 24 petri dishes were
es containing 5 mL of filtered seawater. One microliter of prepared, and 10 Enoplolaimus spp. in each petri dish were
each size of microplastic (10 µm, 5 µm, 1 µm, and 0.5 µm) placed in 5 mL of seawater containing microplastics of
was added to each of four petri dishes containing live each size (10, 5, 1, and 0.5 µm). There were six petri dishes
Enoplolaimus spp. (i.e., there were four replicates for each for each microplastic size. The petri dishes were stored
microplastic size). The petri dishes were stored at 20°C at 20°C in the dark. After 48 h of microplastic ingestion,112 T. Kang et al.
Fig. 3. Microplastic intake rate (%) of Enoplolaimus spp. for
Fig. 2. Images of Enoplolaimus spp. ingesting microplastics of different microplastic particle-size treatments. Error bars represent
different sizes. standard deviation.
the ingestion rate of Enoplolaimus spp. in two petri dishes sis, PIngestion and egestion of MPs by marine nematodes 113
Table 1. The abundance of nematodes that ingested microplastics by genus in different microplastic-size treatments.
Nematodes Feeding 10 µm 5 µm 1 µm 0.5 µm
(spp.) type Avg. Ind. MP Ingest. Avg. Ind. MP Ingest. Avg. Ind. MP Ingest. Avg. Ind. MP Ingest.
Metachromodora 2B 37.0 0.0 50.0 9.3 71.0 65.3 74.0 73.0
Enoplolaimus 2B 48.7 10.0 32.7 12.3 14.0 13.3 11.7 11.7
Daptonema 1B 17.0 0.3 3.3 1.7 1.0 0.7 0.3 0.3
Enoploides 2B 11.3 1.3 5.0 2.7 3.7 3.3 1.3 1.3
Enoplus 2B 2.7 0.0 3.0 1.3 3.3 3.3 0.3 0.3
Oncholaimus 2B 2.3 0.0 0.7 0.3 1.0 1.0
Araeolaimus 1A 1.0 0.7 0.7 0.7
Halalaimus 1A 1.0 0.0 0.3 0.3
Anoplostoma 1B 0.7 0.0 0.3 0.3
Theristus 1B 0.7 0.0
Polysigma 2A 0.7 0.0
Total 121.0 11.7 95.7 27.7 95.7 88.3 88.3 87.3
Percentage (%) 9.6 28.9 92.3 98.9
Avg. Ind.: Average number of individuals (average for three replicates). MP Ingest.: Average number of individuals that ingested microplas-
tics. 1A, selective deposit feeders; 1B, non-selective deposit feeders; 2A, epistrate feeders; and 2B, predators/omnivores.
Fig. 4. Microplastic intake rate (%) of nematodes depending on
microplastic size and feeding type. Error bars represent standard
deviation. Fig. 5. Proportion of Enoplolaimus spp. containing microplastic
particles in different microplastic particle-size treatments and after
transfer to filtered seawater.
other nematodes is shown in Table 1.
found tended to decrease regardless of particle size. We
Experiment 3-Excretion of microplastics by Enoplolaimus also identified the location of microplastics in the body of
spp. Enoplolaimus spp. The microplastics were found close to
After transferring Enoplolaimus spp. that had ingested the head of Enoplolaimus spp. after 48 h exposure to the
microplastics to filtered seawater, the proportion of indi- microplastic environment; 72 h after being transferred to
viduals in which microplastics were found decreased (Fig. filtered seawater, the microplastics were closer to the tail
5, Table 2). This decrease was attributed to the egestion of (Fig. 6).
microplastics. The proportion of Enoplolaimus spp. with
microplastics was 52.7% at 10 µm, 64.3% at 5 µm, 73.2%
Discussion
at 1 µm, and 88.2% at 0.5 µm after 48 h in a petri dish with
microplastics. After transfer to and incubation in filtered In this study, we investigated the extent to which mi-
seawater for 24 h, the proportion of Enoplolaimus spp. croplastics are ingested by nematodes (in particular
with microplastics was 43.7% at 10 µm, 50.0% at 5 µm, Enoplolaimus spp.) collected from Mallipo Beach in South
74.1% at 1 µm, and 79.2% at 0.5 µm. After transfer to and Korea. We showed that microplastics were ingested by
incubation in filtered seawater for 72 h, the proportion of free-living nematodes collected in the marine environment
Enoplolaimus spp. with microplastics was 48.3% at 10 µm, by using laboratory microcosm experiments. Few stud-
58.3% at 5 µm, 66.7% at 1 µm, and 75.0% at 0.5 µm. The ies have demonstrated that free-living marine nematodes
proportion of individuals in which microplastics were consume microplastics. However, there have been several114 T. Kang et al.
Table 2. The percentage (%) of Enoplolaimus spp. that have microplastic in different microplastic-size treatments and after transfer to
filtered seawater.
Size (µm) Replication Microplastic ingestion rate (48 h) 24 h in filtered seawater 72 h in filtered seawater
a 42.9 42.9 16.7
10 b 62.5 44.4 80.0
Avg. 52.7 43.7 48.3
a 57.1 25.0 50.0
5 b 71.4 75.0 66.7
Avg. 64.3 50.0 58.3
a 71.4 62.5 66.7
1 b 75.0 85.7 66.7
Avg. 73.2 74.1 66.7
a 88.9 75.0 80.0
0.5 b 87.5 83.3 70.0
Avg. 88.2 79.2 75.0
lation of microplastics through food chains in the marine
environment. However, lower trophic organisms, such as
invertebrates, likely ingest and accumulate microplastics,
introducing them to the food chains of the marine environ-
ment (Wright et al. 2013a).
In Experiment 2, we showed that the size of microplas-
tics, rather than feeding type of nematodes, affected inges-
Fig. 6. Image of microplastics in the intestines of Enoplolaimus tion rates. The size and shape of microplastics, exposure
spp. A, exposure to plastic environment; B, 72 h after transfer to concentration and time, morphological features of nema-
filtered seawater. todes (e.g., buccal cavity size and intestine dimensions),
and species-specific feeding habits probably constrain the
recent studies investigating microplastic ingestion by one uptake and ingestion of microplastics by nematodes (Gray
freshwater nematode species, C. elegans (Zhao et al. 2017, & Weinstein 2017, Lehtiniemi et al. 2018, Fueser et al.
Lei et al. 2018, Fueser et al. 2019). C. elegans worms ac- 2019). Most nematodes collected in natural sediments for
tively accumulate 0.5 and 1 µm fluorescent polystyrene mi- this experiment were predators/omnivores. Additionally,
crospheres in the presence and absence of bacterial food, selective deposit feeders and non-selective deposit feeders
whereas microspheres of 3 µm are rarely appeared with low abundance. However, few nematodes
accumulated (Kiyama et al. 2012). were of the epistrate feeding type. For this reason, the
In the current study, Experiment 1 showed that smaller results of non-predator/omnivore feeding-type nematodes
microplastics were more often detected in Enoplolaimus may not have been reflected well. In contrast, the size of
spp. bodies than larger microplastics. The reason for this microplastics had a great influence on the intake rate. The
result could be that given the smaller the size of the mi- small size of microplastics is an important factor affect-
croplastics and the higher the number of microplastics ing bioavailability, particularly for lower trophic organisms
particles added to the petri dishes, these small microplas- (Wright et al. 2013a). The ingestion of microplastics by
tics have a higher probability of entering the mouth of nematodes is predominantly determined by their feeding
nematodes than large microplastics. Previous studies have habits and can be predicted by the morphology of the buc-
reported that the size of microplastics influences the likeli- cal cavity. Fueser et al. (2019) showed that feeding habit
hood of ingestion. For example, a review paper summariz- and the buccal cavity of nematodes have larger effects than
ing microplastic studies conducted on various organisms other factors (such as species-specific feeding differences,
showed that ingestion depends on the size of microplastic exposure time, and exposure concentration) on the inges-
particles, among other factors (Phuong et al. 2016). Lehti- tion of microplastics and could be important for control-
niemi et al. (2018) showed that the size of microplastic ling the quantity of microplastic uptake.
particles, rather than shape, strongly influences the amount In Experiment 3, we investigated whether the microplas-
of microplastics ingested in an experiment using fish and tic particles were retained in the bodies of Enoplolaimus
mysid shrimps. Few studies have evaluated the bioaccumu- spp. or egested. The excretion of microplastics by macroor-Ingestion and egestion of MPs by marine nematodes 115
ganisms has been investigated by measuring the ingestion of microplastics by macroorganisms. For example, Gra-
of microplastic particles and quantifying the microplastics ham et al. (2019) showed that pacific oysters have effi-
in fecal debris. For example, Graham & Thompson (2009) cient egestion rates of microplastics (84.6±2%) and Van
quantified the excretion of microplastics by four species Cauwenberghe et al. (2015a), who analyzed the fecal casts
of sea cucumber. However, it is more difficult to quantify of Polychaeta, showed that they excrete some microplastic
the excretion of microplastics by microorganisms such as particles.
marine nematodes. Therefore, in this study, we first deter- Nematodes are widely distributed globally, including in
mined the proportion of nematodes that ingested micro- extreme environments (such as in polar, deep-sea, and hy-
plastics and then determined the proportion of nematodes drothermal areas). Microplastics are also widely distrib-
that still contained microplastics after being transferred to uted in the marine environment; thus, they are available
and incubated in filtered seawater for 24 h or 72 h. to nematodes. Our study showed that sunk microplastics
The proportion of Enoplolaimus spp. with 10 µm micro- are ingested by nematodes living in marine benthic eco-
plastics in the body decreased by 4.4 percentage points, systems. In these experiments, conducted on Enplolaimus
that with 5 µm microplastics decreased by 6.0 percent- spp., which have a large mouth, the microplastics of the
age points, that with 1 µm microplastics decreased by 6.5 sizes used in this study could be sufficiently ingested. As a
percentage points, and that with 0.5 µm microplastics de- result, microplastics of all sizes were identified in the body
creased by 13.2 percentage points after 72 hours. When the of nematodes. In addition, since the number of nematodes
size of the microplastic decreased, it was expected that mi- used in Experiment 2 by feeding type is small, the dif-
croplastics would easily escape from the body along the di- ference in the ingestion rate of the nematode, depending
gestive tract; however, this effect cannot be identified sig- on the feeding type is not clear. However, the intake rate
nificantly differently due to the lack of sufficient samples to can be expected to be more affected by the size of the mi-
achieve relevant statistical power. Also, in Experiment 3, croplastics rather than the difference in feeding types. In
we transferred the nematodes to the filtered seawater and Experiment 3, contrary to expectations, the discharge rate
checked the discharge of microplastics for just three days. of microplastics into the body of nematodes according to
After three days of experiments in filtered sea water, we the size of microplastics could not be detected. After trans-
observed that the transferred nematodes slowed down and ferring Enoplolaimus spp. to filtered seawater, the propor-
their health condition deteriorated, therefore, we no longer tion of nematodes containing the smallest size microplas-
proceeded with the experiments. However, we expected tic (0.5 µm) decreased by 15% of the ingested amount in
that the egestion rates of microplastics would increase fur- 3 days. As microplastics sink through the water column
ther if the nematode is provided conditions to maintain a when they become covered with biofilm, eventually set-
healthy state in the petri dish for more than three days. Be- tling onto sediments (Wright et al. 2013a), the microplas-
cause the intestinal tract of nematodes is a simple, hollow, tics ingested by nematodes will likely be transferred to
straight tube consisting of a single layer of epithelial cells, animals that feed on them. Future studies should evaluate
it is not difficult to move any sized microplastic from the how microplastics are transmitted and how they accumu-
mouth to the anus (Basyoni & Rizk 2016). Recently, Fue- late within the benthic food web.
ser et al. (2020) showed that the two nematode species, C.
elegans and P. pacificus, rapidly ingest and egest PS beads
Acknowledgements
(0.5 and 1.0 µm) along with bacteria. These two nematodes
are not free-living marine nematodes, but the results are This research was a part of the project titled “Under-
very important in relation to the bioconcentration of mi- standing the deep-sea biosphere on seafloor hydrothermal
croplastics. vents in the Indian Ridge” (No. 20170411), funded by the
Finally, we checked the location of microplastics in the Ministry of Oceans and Fisheries, Korea.
body of Enoplolaimus spp. In Experiment 1, the location of
microplastics in the body of Enoplolaimus spp. was mostly
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